Wnt Signaling through the Ror Receptor in the Nervous System

Molecular Neurobiology

Volumn 49, Issue 1, 2014, Pages 303-315

  Petrova, Iveta M ^a   Malessy, Martijn J ^a   Verhaagen, Joost ^b   Fradkin, Lee G ^a   Noordermeer, Jasprina N ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

Axonal Branching and Pruning; CNS; Neuronal Migration; Ror; Synapse; Wnt

Indexed keywords

DISHEVELLED PROTEIN; FRIZZLED PROTEIN; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR 1; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR 2; UNCLASSIFIED DRUG;

APLYSIA CALIFORNICA; CAENORHABDITIS ELEGANS; CELL MIGRATION; DROSOPHILA MELANOGASTER; HUMAN; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; WNT SIGNALING PATHWAY; XENOPUS LAEVIS; ZEBRA FISH;

ANIMALS; CELL MOVEMENT; HUMANS; NERVOUS SYSTEM; RECEPTOR TYROSINE KINASE-LIKE ORPHAN RECEPTORS; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY;

EID: 84894319378     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8520-9     Document Type: Review

References (111)

1. Blume-Jensen P, Hunter T (2001) Oncogenic kinase signalling. Nature 411(6835):355-365
2. Lemmon MA, Schlessinger J (2010) Cell signaling by receptor tyrosine kinases. Cell 141(7):1117-1134
3. Klein R et al (1989) trkB, a novel tyrosine protein kinase receptor expressed during mouse neural development. EMBO J 8(12):3701-3709
4. Seger R, Rodeck U, Yarden Y (2008) Receptor tyrosine kinases: the emerging tip of systems control. IET Syst Biol 2(1):1-4
5. Masiakowski P, Carroll RD (1992) A novel family of cell surface receptors with tyrosine kinase-like domain. J Biol Chem 267(36):26181-26190
6. McKay SE et al (2001) Aplysia ror forms clusters on the surface of identified neuroendocrine cells. Mol Cell Neurosci 17(5):821-841
7. Jennings CG, Dyer SM, Burden SJ (1993) Muscle-specific trk-related receptor with a kringle domain defines a distinct class of receptor tyrosine kinases. Proc Natl Acad Sci U S A 90(7):2895-2899
8. Wilson C, Goberdhan DC, Steller H (1993) Dror, a potential neurotrophic receptor gene, encodes a Drosophila homolog of the vertebrate Ror family of Trk-related receptor tyrosine kinases. Proc Natl Acad Sci U S A 90(15):7109-7113
9. Oishi I et al (1997) A novel Drosophila receptor tyrosine kinase expressed specifically in the nervous system. Unique structural features and implication in developmental signaling. J Biol Chem 272(18):11916-11923
10. Hikasa H et al (2002) The Xenopus receptor tyrosine kinase Xror2 modulates morphogenetic movements of the axial mesoderm and neuroectoderm via Wnt signaling. Development 129(22):5227-5239
11. Oishi I et al (1999) Spatio-temporally regulated expression of receptor tyrosine kinases, mRor1, mRor2, during mouse development: implications in development and function of the nervous system. Genes Cells 4(1):41-56
12. Paganoni S, Anderson KL, Ferreira A (2004) Differential subcellular localization of Ror tyrosine kinase receptors in cultured astrocytes. Glia 46(4):456-466
13. Forrester WC et al (1999) A C. elegans Ror receptor tyrosine kinase regulates cell motility and asymmetric cell division. Nature 400(6747):881-885
14. Koga M et al (1999) Control of DAF-7 TGF-(alpha) expression and neuronal process development by a receptor tyrosine kinase KIN-8 in Caenorhabditis elegans. Development 126(23):5387-5398
15. Xu YK, Nusse R (1998) The frizzled CRD domain is conserved in diverse proteins including several receptor tyrosine kinases. Curr Biol 8(12):R405-R406
16. Masiakowski P, Yancopoulos GD (1998) The Wnt receptor CRD domain is also found in MuSK and related orphan receptor tyrosine kinases. Curr Biol 8(12):R407
17. Wang Y et al (1996) A large family of putative transmembrane receptors homologous to the product of the Drosophila tissue polarity gene frizzled. J Biol Chem 271(8):4468-4476
18. Bhanot P et al (1996) A new member of the frizzled family from Drosophila functions as a wingless receptor. Nature 382(6588):225-230
19. Oishi I et al (2003) The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8(7):645-654
20. Forrester WC, Kim C, Garriga G (2004) The Caenorhabditis elegans Ror RTK CAM-1 inhibits EGL-20/Wnt signaling in cell migration. Genetics 168(4):1951-1962
21. Kani S et al (2004) The receptor tyrosine kinase Ror2 associates with and is activated by casein kinase Iepsilon. The Journal of Biological Chemistry 279(48):50102-50109
22. Billiard J et al (2005) The orphan receptor tyrosine kinase Ror2 modulates canonical Wnt signaling in osteoblastic cells. Mol Endocrinol 19(1):90-101
23. Mikels AJ, Nusse R (2006) Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol 4(4):e115
24. Green JL, Inoue T, Sternberg PW (2007) The C. elegans ROR receptor tyrosine kinase, CAM-1, non-autonomously inhibits the Wnt pathway. Development 134(22):4053-4062
25. Zinovyeva AY et al (2008) Complex network of Wnt signaling regulates neuronal migrations during Caenorhabditis elegans development. Genetics 179(3):1357-1371
26. Paganoni S, Bernstein J, Ferreira A (2010) Ror1-Ror2 complexes modulate synapse formation in hippocampal neurons. Neuroscience 165(4):1261-1274
27. Jensen M et al (2012) Wnt signaling regulates acetylcholine receptor translocation and synaptic plasticity in the adult nervous system. Cell 149(1):173-187
28. Williams AF, Barclay AN (1988) The immunoglobulin superfamily - domains for cell surface recognition. Annu Rev Immunol 6:381-405
29. Chao MV (1992) Neurotrophin receptors: a window into neuronal differentiation. Neuron 9(4):583-593
30. Melkonyan HS et al (1997) SARPs: a family of secreted apoptosis-related proteins. Proc Natl Acad Sci U S A 94(25):13636-13641
31. Saldanha J, Singh J, Mahadevan D (1998) Identification of a frizzled-like cysteine rich domain in the extracellular region of developmental receptor tyrosine kinases. Protein Sci 7(8):1632-1635
32. Forrester WC (2002) The Ror receptor tyrosine kinase family. Cell Mol Life Sci 59(1):83-96
33. Furie B, Furie BC (1988) The molecular basis of blood coagulation. Cell 53(4):505-518
34. Patthy L (1985) Evolution of the proteases of blood - coagulation and fibrinolysis by assembly from modules. Cell 41(3):657-663
35. Yamamoto H et al (2007) Wnt5a modulates glycogen synthase kinase 3 to induce phosphorylation of receptor tyrosine kinase Ror2. Genes to Cells: Devoted to Molecular & Cellular Mechanisms 12(11):1215-1223
36. Liu Y et al (2008) Wnt5a induces homodimerization and activation of Ror2 receptor tyrosine kinase. J Cell Biochem 105(2):497-502
37. Pearson RB, Kemp BE (1991) Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol 200:62-81
38. Cunningham ME et al (1997) Autophosphorylation of activation loop tyrosines regulates signaling by the TRK nerve growth factor receptor. J Biol Chem 272(16):10957-10967
39. Songyang Z, Cantley LC (1995) Recognition and specificity in protein tyrosine kinase-mediated signalling. Trends Biochem Sci 20(11):470-475
40. Mikels A, Minami Y, Nusse R (2009) Ror2 receptor requires tyrosine kinase activity to mediate Wnt5A signaling. The Journal of Biological Chemistry 284(44):30167-30176
41. Enomoto M et al (2009) Autonomous regulation of osteosarcoma cell invasiveness by Wnt5a/Ror2 signaling. Oncogene 28(36):3197-3208
42. Akbarzadeh S et al (2008) The deleted in brachydactyly B domain of ROR2 is required for receptor activation by recruitment of Src. PloS one 3(3):e1873
43. Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241(4861):42-52
44. Boudeau J et al (2006) Emerging roles of pseudokinases. Trends Cell Biol 16(9):443-452
45. Gentile A et al (2011) Ror1 is a pseudokinase that is crucial for Met-driven tumorigenesis. Cancer Res 71(8):3132-3141
46. Cadigan KM, Nusse R (1997) Wnt signaling: a common theme in animal development. Genes & Develop 11(24):3286-3305
47. Koles K, Budnik V (2012) Wnt signaling in neuromuscular junction development. Cold Spring Harb Perspect Biol 4(6):a008045
48. Salinas PC (2012) Wnt signaling in the vertebrate central nervous system: from axon guidance to synaptic function. Cold Spring Harb Perspect Biol 4(2):a008003
49. Budnik V, Salinas PC (2011) Wnt signaling during synaptic development and plasticity. Curr Opin Neurobiol 21(1):151-159
50. Salinas PC, Zou Y (2008) Wnt signaling in neural circuit assembly. Annu Rev Neurosci 31:339-358
51. Park M, Shen K (2012) WNTs in synapse formation and neuronal circuitry. EMBO J 31(12):2697-2704
52. Clevers H, Nusse R (2012) Wnt/beta-catenin signaling and disease. Cell 149(6):1192-1205
53. Simons M, Mlodzik M (2008) Planar cell polarity signaling: from fly development to human disease. Annu Rev Genet 42:517-540
54. Kohn AD, Moon RT (2005) Wnt and calcium signaling: beta-catenin- independent pathways. Cell Calcium 38(3-4):439-446
55. Fradkin LG, Dura JM, Noordermeer JN (2010) Ryks: new partners for Wnts in the developing and regenerating nervous system. Trends Neurosci 33(2):84-92
56. Halford MM et al (2000) Ryk-deficient mice exhibit craniofacial defects associated with perturbed Eph receptor crosstalk. Nat Genet 25(4):414-418
57. Ho HY et al. (2012) Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proceedings of the National Academy of Sciences of the United States of America
58. Afzal AR et al (2000) Recessive Robinow syndrome, allelic to dominant brachydactyly type B, is caused by mutation of ROR2. Nat Genet 25(4):419-422
59. Afzal AR, Jeffery S (2003) One gene, two phenotypes: ROR2 mutations in autosomal recessive Robinow syndrome and autosomal dominant brachydactyly type B. Hum Mutat 22(1):1-11
60. Oldridge M et al (2000) Dominant mutations in ROR2, encoding an orphan receptor tyrosine kinase, cause brachydactyly type B. Nat Genet 24(3):275-278
61. van Bokhoven H et al (2000) Mutation of the gene encoding the ROR2 tyrosine kinase causes autosomal recessive Robinow syndrome. Nat Genet 25(4):423-426
62. Schwabe GC et al (2000) Distinct mutations in the receptor tyrosine kinase gene ROR2 cause brachydactyly type B. Am J Hum Genet 67(4):822-831
63. Robinow M, Silverman FN, Smith HD (1969) A newly recognized dwarfing syndrome. Am J Dis Child 117(6):645-651
64. Butler MG, Wadlington WB (1987) Robinow syndrome: report of two patients and review of literature. Clin Genet 31(2):77-85
65. Soliman AT et al (1998) Recessive Robinow syndrome: with emphasis on endocrine functions. Metabolism 47(11):1337-1343
66. Teebi AS (1990) Autosomal recessive Robinow syndrome. Am J Med Genet 35(1):64-68
67. Takeuchi S et al (2000) Mouse Ror2 receptor tyrosine kinase is required for the heart development and limb formation. Genes Cells 5(1):71-78
68. Liu Y, Bodine PV, Billiard J (2007) Ror2, a novel modulator of osteogenesis. Journal of Musculoskeletal & Neuronal Interactions 7(4):323-324
69. Liu Y et al (2007) Homodimerization of Ror2 tyrosine kinase receptor induces 14-3-3(beta) phosphorylation and promotes osteoblast differentiation and bone formation. Mol Endocrinol 21(12):3050-3061
70. Nomi M et al (2001) Loss of mRor1 enhances the heart and skeletal abnormalities in mRor2-deficient mice: redundant and pleiotropic functions of mRor1 and mRor2 receptor tyrosine kinases. Mol Cell Biol 21(24):8329-8335
71. Maeda K et al (2012) Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nature Medicine 18(3):405-412
72. Daneshmanesh AH et al (2012) Orphan receptor tyrosine kinases ROR1 and ROR2 in hematological malignancies. Leuk Lymphoma 54(4):843-850
73. Francis MM et al (2005) The Ror receptor tyrosine kinase CAM-1 is required for ACR-16-mediated synaptic transmission at the C. elegans neuromuscular junction. Neuron 46(4):581-594
74. Lamballe F, Klein R, Barbacid M (1991) trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66(5):967-979
75. Green JL, Kuntz SG, Sternberg PW (2008) Ror receptor tyrosine kinases: orphans no more. Trends Cell Biol 18(11):536-544
76. Sossin WS (2006) Tracing the evolution and function of the Trk superfamily of receptor tyrosine kinases. Brain, Behavior and Evolution 68(3):145-156
77. Katoh M (2005) Comparative genomics on ROR1 and ROR2 orthologs. Oncology Reports 14(5):1381-1384
78. Sudol M (1996) The WW module competes with the SH3 domain? Trends Biochem Sci 21(5):161-163
79. Matsuda T et al (2001) Expression of the receptor tyrosine kinase genes, Ror1 and Ror2, during mouse development. Mech Dev 105(1-2):153-156
80. Paganoni S, Ferreira A (2003) Expression and subcellular localization of Ror tyrosine kinase receptors are developmentally regulated in cultured hippocampal neurons. J Neurosci Res 73(4):429-440
81. Al-Shawi R et al (2001) Expression of the Ror1 and Ror2 receptor tyrosine kinase genes during mouse development. Dev Genes Evol 211(4):161-171
82. Endo M, Doi R, Nishita M, Minami Y (2012) Ror family receptor tyrosine kinases regulate the maintenance of neural progenitor cells in the developing neocortex. J Cell Sci 125(Pt 8):2017-2029
83. Forrester WC, Garriga G (1997) Genes necessary for C. elegans cell and growth cone migrations. Development 124(9):1831-1843
84. Kim C, Forrester WC (2003) Functional analysis of the domains of the C. elegans Ror receptor tyrosine kinase CAM-1. Dev Biol 264(2):376-390
85. Modzelewska K et al (2013) Neurons refine the Caenorhabditis elegans body plan by directing axial patterning by Wnts. PLoS Biology 11(1):e1001465
86. Green JL, Inoue T, Sternberg PW (2008) Opposing Wnt pathways orient cell polarity during organogenesis. Cell 134(4):646-656
87. Sulston JE et al (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100(1):64-119
88. Song S et al (2010) A Wnt-Frz/Ror-Dsh pathway regulates neurite outgrowth in Caenorhabditis elegans. PLoS Genet 6(8):e1001056
89. Paganoni S, Ferreira A (2005) Neurite extension in central neurons: a novel role for the receptor tyrosine kinases Ror1 and Ror2. J Cell Sci 118(Pt 2):433-446
90. Yoda A, Oishi I, Minami Y (2003) Expression and function of the Ror-family receptor tyrosine kinases during development: lessons from genetic analyses of nematodes, mice, and humans. J Recept Signal Transduct Res 23(1):1-15
91. Ferreira A, Busciglio J, Caceres A (1989) Microtubule formation and neurite growth in cerebellar macroneurons which develop in vitro: evidence for the involvement of the microtubule-associated proteins, MAP-1a, HMW-MAP2 and Tau. Brain Res Dev Brain Res 49(2):215-228
92. Caceres A, Kosik KS (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343(6257):461-463
93. Caceres A, Mautino J, Kosik KS (1992) Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron 9(4):607-618
94. Avila J, Dominguez J, Diaznido J (1994) Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int J Dev Biol 38(1):13-25
95. Holgado A, Ferreira A (2000) Synapse formation proceeds independently of dendritic elongation in cultured hippocampal neurons. J Neurobiol 43(2):121-131
96. Gonzalez-Billault C et al (2002) Participation of structural microtubule-associated proteins (MAPs) in the development of neuronal polarity. J Neurosci Res 67(6):713-719
97. Wilson TE et al (1993) A genetic method for defining DNA-binding domains: application to the nuclear receptor NGFI-B. Proc Natl Acad Sci U S A 90(19):9186-9190
98. Djiane A et al (2000) Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 127(14):3091-3100
99. Ku M, Melton DA (1993) Xwnt-11: a maternally expressed Xenopus wnt gene. Development 119(4):1161-1173
100. Tada M, Smith JC (2000) Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via dishevelled, but not through the canonical Wnt pathway. Development 127(10):2227-2238
101. Hayashi Y et al (2009) A trophic role for Wnt-Ror kinase signaling during developmental pruning in Caenorhabditis elegans. Nat Neurosci 12(8):981-987
102. Nishita M et al (2010) Ror2/Frizzled complex mediates Wnt5a-induced AP-1 activation by regulating dishevelled polymerization. Mol Cell Biol 30(14):3610-3619
103. Kennerdell JR, Fetter RD, Bargmann CI (2009) Wnt-Ror signaling to SIA and SIB neurons directs anterior axon guidance and nerve ring placement in C. elegans. Development 136(22):3801-3810
104. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314(1165):1-340
105. Babu K et al (2011) The immunoglobulin super family protein RIG-3 prevents synaptic potentiation and regulates Wnt signaling. Neuron 71(1):103-116
106. Malessy MJ, Pondaag W (2009) Obstetric brachial plexus injuries. Neurosurgery Clinics of North America 20(1):1-14, v
107. Sato A et al (2010) Wnt5a regulates distinct signalling pathways by binding to Frizzled2. The EMBO Journal 29(1):41-54
108. Henriquez JP et al (2008) Wnt signaling promotes AChR aggregation at the neuromuscular synapse in collaboration with agrin. Proc Natl Acad Sci U S A 105(48):18812-18817
109. Wu H, Xiong WC, Mei L (2010) To build a synapse: signaling pathways in neuromuscular junction assembly. Development 137(7):1017-1033
110. Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98(2):81-85
111. Feike AC et al (2010) Wnt5a/Ror2-induced upregulation of xPAPC requires xShcA. Biochem Biophys Res Commun 400(4):500-506